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Antifouling Adaptations of Marine Shrimp (Decapoda: Caridea): Gill Cleaning Mechanisms and Grooming of Brooded Embryos

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Antifouling Adaptations of Marine Shrimp (Decapoda: Caridea): Gill Cleaning Mechanisms and Grooming of Brooded Embryos Zoological Journal oj the Linnean Society, 6i: 281-305. With 12 figures April 1979 Antifouling adaptations of marine shrimp (Decapoda: Caridea): gill cleaning mechanisms and grooming of brooded embryos RAYMOND T. BAUER Biological Sciences, California Polytechnic State University, San Luis Obispo, California, U.S.A. Accepted for publication September 1977 Gills in the branchial chambers of caridean shrimps, as well as the brooded embryos in females, are subject to fouling by particulate debris and epizoites. Important mechanisms for cleaning the gills are brushing of the gills by the grooming or cleaning chelipeds in some species, while in others, setae from the bases of the thoracic legs brush up among the gills during movement of the limbs (epipod- setobranch complexes). Setae of cleaning chelipeds and of epipod-setobranch complexes show- similar ultrastructural adaptions for scraping gill surfaces. Ablation of the cleaning chelipeds ol the shrimp Heptacarpm pictus results in severe fouling of the gills in experimenials, while those of controls remain clean, Embrvos brooded by female carideans are often brushed and jostled by the grooming chelipeds. In H. pictui. removal of the cleaning chelae results in heavier microbial and sediment fouling than in controls. KEY WO RDS: - shrimp - gills - grooming - cleaning - cpipods - sctobranchs - fouling - Decapoda - Caridea. CONTENTS Introduction 281 Methods 282 Results 284 Gill cleaning by the chelipeds 284 Gill cleaning by the epipod-setobranch complex 289 Experiments on the adaptive value of cheliped brushing in Heptacarpus pictus 292 Cleaning of brooded embryos 296 Experiments on the adaptive value of cheliped brushing of eggs in Heptacarpus pictus 297 Discussion 299 Adaptive value of gill cleaning mechanisms in caridean shrimp 299 Adaptive value of embryo brushing by females 301 Acknowledgements 302 References 302 INTRODUCTION Grooming behaviour is a frequent activity of caridean shrimp which appears to prevent epizoic and sediment fouling of the body (Bauer, 1975; Bauer, 1977, Bauer, 1978). This report deals with two specialized components of grooming behaviour, gill cleaning and female care of brooded embryos. The functional 281 0O24-4O82/79/O40281-2S/SO2.OO/O © 1979 The Linnean Society of London 16 •is-i R. I'. BAUER morphology of these behaviours and the ultrastructure of setae and processes utilized in these behaviours is'described. Experiments were performed which suggest the adaptive value of these behaviours. Gills of caridean shrimp, like those of other decapod crustaceans, are enclosed within a branchial chamber. Gills are thus protected from injury while a rapid How of water can be drawn across them in the narrow chamber by the pumping action of the scaphognathite (gill bailer). However, the enclosure of the gills creates a disadvantage in that gill lamellae in a confined space form a sediment trap. Particulate matter borne by the respiratory current can collect among gill filaments. Since the gills are thin outgrowths of the exoskeleton, there can be no ciliary-mucoid mechanisms to entrap and carry away this sediment, as in corals for example. In addition, fouling organisms might grow on and smother respiratory surfaces. Perhaps in response to these environmental pressures, it appears that carideans and other decapods have evolved a number of mechanisms to retard or prevent fouling. Although Vuillemin (1967) has discussed methods of gill cleaning in the Decapoda, those of caridean shrimp have not been studied in any detail. In this study, two major gill cleaning mechanisms of the Caridea were investigated: active brushing of the gills by the cleaning chelipeds and passive brushing by the epipod-setobranch system. Female caridean shrimp, like other decapod crustaceans (except the Penaeidea), carry developing embryos attached beneath the abdomen which, in marine lorms, hatch as advanced planktonic larvae. One possible function of incubation is to protect the embryos from predation and chance environmental injury to which the eggs and larvae of copiously spawning invertebrates such as coelenterates and echinoderms are subjected. Most decapods exhibit some sort of parental care in aeration and cleaning of embryos which can be termed brooding behaviour. Like the gills, the mass of embryos serves as a filter which accumulates debris from water circulating through them. In several species of shrimp, females pick and brush among the mass of embryos with the cleaning chelipeds. In this study, the survival value of this component of brooding behaviour was investigated in a caridean species, Heptacarpus pictus (Stimpson). Observations on brushing of the gills by cleaning chelipeds in Caridea have been reported for various palaemonid species (Doflein, 1910; Schone, 1961), and lor the gnathophyllid Hymenocera picla Dana (Wickler 8c Seibt, 1970). A study on brooding behaviour in a caridean has been conducted by Phillips (1971) [Palaemon serratus (Pennant)). METHODS Nineteen species of caridean shrimp were observed alive in this study, chiefly in laboratory seawater aquaria (Table 1). If the shrimps were small, it was convenient to observe cleaning behaviour through a hand-held dissecting microscope. Grooming activities were recorded by light photography. Transparencies made with a 35 mm camera using an electronic flash of 1/1500 sec duration could record the exact position of limbs during grooming. Drawings of die various behaviours were made by projecting the transparencies on to paper, where they were traced. Information on the location of collection and the time spent observing each species can be found in a previous report on antennular preening in Caridea (Bauer, 1977). SHRIMP ANTIFOULING ADAPTATIONS 288 Table 1. Gill cleaning mechanisms of caridean species observed alive (+, present; —, absent) Brushing by Epipod - sciobranch Species cleaning chelipeds systems Alpheidae Hclaeus macginitieae Han + 6. harfordi (Kingsley) + Alpliem sp. (from San Diego) Alpheui sp. (from San Felipe. Baja California) Crangonidae Crangon nigriaiuda Siimpson I'aracrangon echmata Dana Hippolyiidae lli-//iiicarpm pictus (Siimpson) + + , reduced //. breviroilrh (Dana) + +, reduced ll.palputvr (Owen) + +, reduced //. paiudicola (Holmes) + +, reduced //. stylus (Siimpson) + H. taytori (Siimpson) + +,reduced Lysmala calijomica Siimpson Palaemonidae Paiaanon niieti Holmes Pandalidae Pmiilalus danne Siimpson Pandalus spp. + I'andalopmdispar Raihhun + Most behavioural observations were made on Heptacarpus pictus (Hippolytidae), a small tidepool species of the southern California coast; Belaeus macginilieae (Alpheidae), a subtidal species commensal with sea urchins; Palaemon rilleri, a tidepool species from the Gulf of California, Baja California; and Pandalus danae, a large subtidal schooling species of the Pacific Northwest. Structure of appendages and processes was recorded by light microscopy with camera lucicla drawings. Infrastructure of glooming setae and processes was recorded with scanning electron microscopy, with the methods outlined in Bauer (1975). In addition to species observed alive, grooming behaviours were inferred from the morphology of several species using preserved material (Table 2). These specimens were largely from the Benthic Invertebrate Museum of the Scripps Institution of Oceanography, where most of this research was carried out. Some preserved material was obtained through the courtesy of the United States National Museum. Experiments on the adaptive value of gill brushing were performed on two species, Heptacarpus pictus and Pandalus danae. In experiments with H. pictus sin imp had the cleaning chelipeds ablated, while controls had the first walking leg removed. Both experimental and controls were placed in 4-5 1 plastic buckets (cages) covered at the top with line plastic mesh and perforated by many 284 R. T. BAUER 2-3 mm holes through which sea-water could circulate. The cages were hung in the settling tanks of the Scripps Insdtution of Oceanography (SIO) seawater system. Seawater flows down the SIO pier in a flume which empties into the settling tanks before filtration and use in the SIO facilities. Attached to the cages were settling plates (standard glass microscope slides and 50 x 70 mm rectangles of asbestos board). Three ablation experiments were conducted: 8—25 February 1974 (25 experimental, 25 controls); 6-19 April 1974 (26 experimental, 26 controls); and 22 July—1 August 1974 (20 experimentals, 20 controls). All individuals were gravid females carrying embryos in the early stages of development. These individuals were chosen to prevent interruption of the experiment by molting (brooding females do not molt) and also to test the effect of a lack of grooming of brooded embryos. At the end of the experiment, the shrimps were preserved in seawater Bouin's solution (first experiment) or 1096 seawater formalin (second and third experiments). To quantify fouling of the gills, gills were removed from the preserved animals, mounted and cleared in Turtox CMC-10 medium, and viewed under a compound microscope at x400 so that the gill filled the entire field of vision. A sensitive exposure meter (Lafayette Model F 49) was used to measure light transmission through the gills. A reading was taken with the gill in (gill reading) and out (blank reading) of the field of vision. Percent transmission is the gill reading/blank reading x 100. A gill reading and a blank reading had to be taken with each gill, due to voltage fluctuations which caused variation in illumination. A similar
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